Abstract
The biological control agent (tamarisk leaf beetle, Diorhabda spp.) is actively being used to defoliate exotic saltcedar or tamarisk (Tamarix spp.) in riparian ecosystems in western USA. The Virgin River in Arizona and Nevada is a system where tamarisk leaf beetle populations are spreading. Saltcedar biocontrol, like other control methods, has the potential to affect non-target species. Because amphibians and reptiles respond to vegetation changes in habitat and forage in areas where beetles are active, herpetofauna are model taxa to investigate potential impacts of biocontrol defoliation. Our objectives related herpetofauna abundance to vegetation cover and indices (normalized difference vegetation index, NDVI; enhanced vegetation index, EVI) and timing of biocontrol defoliation. We captured herpetofauna and ground-dwelling arthropods in trap arrays and measured vegetation using remotely sensed images and on-the-ground measurements at 16–21 sites 2 years before (2009–2010) and 2 years following (2011–2012) biocontrol defoliation. Following defoliation, riparian stands (including stands mixed with native and exotic trees and stands of monotypic exotic saltcedar) had significantly lower NDVI and EVI values and fewer captures of marked lizards. Total captures of herpetofauna (toads, lizards, and snakes) were related to higher vegetation cover and sites with a lower proportion of saltcedar. Our results suggest that effects of biocontrol defoliation are likely to be site-specific and depend upon the proportion of native riparian trees established prior to biocontrol introduction and defoliation. The mechanisms by which habitat structure, microclimate, and ultimately vertebrate species are affected by exotic plant biocontrol riparian areas should be a focus of natural-resource managers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Angilletta MJ, Sears MW, Pringle RM (2009) The spatial dynamics of nesting behavior: lizards shift microhabitats to construct nests with beneficial thermal properties. Ecology 90:2933–2939
Bateman HL, Ostoja SM (2012) Invasive woody plants affect the composition of native lizard and small mammal communities in riparian woodlands. Anim Conserv 15:294–304
Bateman HL, Chung-MacCoubrey A, Snell HL (2008) Impact of non-native plant removal on lizards in riparian habitats in the southwestern United States. Restor Ecol 16:180–190
Bateman HL, Dudley TL, Bean DW, Ostoja SM, Hultine KR, Kuehn MJ (2010) A river system to watch: documenting the effects of saltcedar (Tamarix spp.) biocontrol in the Virgin River Valley. Ecol Restor 28:405–410
Bateman HL, Nagler PL, Glenn EP (2013a) Plot- and landscape-level changes in climate and vegetation following defoliation of exotic saltcedar (Tamarix sp.) from the biocontrol agent Diorhabda carinulata along a stream in the Mojave Desert (USA). J Arid Environ 89:16–20
Bateman HL, Paxton EH, Longland WS (2013b) Tamarix as wildlife habitat. In: Sher A, Quigley M (eds) Tamarix: passenger vs. driver of ecological change. Oxford University Press, UK, pp 168–188
Bennett FD, Hughes IW (1959) Biological control of insect pests in Bermuda. Bull Entomol Res 50:423–436
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
Crother BI et al (2012) Scientific and standard English names of amphibians and reptiles of North America north of Mexico, with comments regarding confidence in our understanding. SSAR Herpetol Circ 37:1–92
DeClercq P, Manson P, Babendreier D (2011) Benefits and risks of exotic biological control agents. Biocontrol 56:681–698
Denslow JS, D’Antonio CM (2005) After biocontrol: assessing indirect effects of insect releases. Biol Control 35:307–318
Follstad Shah JJ, Dahm CN, Gloss SP, Bernhardt ES (2007) River and riparian restoration in the southwest: results of the national river restoration science synthesis project. Restor Ecol 15:550–562
Friedman J, Auble G, Shafroth P, Scott M, Merigliano M, Freehling M, Griffen E (2005) Dominance of non-native riparian trees in western USA. Biol Invasions 7:747–751
Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in US invasion and undetected in native Asian range. Proc Natl Acad Sci 99:11256–11259
Gaskin JF, Schaal BA (2003) Molecular phylogenetic investigation of US invasive Tamarix. Syst Bot 28:86–95
Greenberg CH, Neary DG, Harris LD (1994) Effects of high-intensity wildfire and silvicultural treatments on reptile communities in sand-pine scrub. Conserv Biol 4:1047–1057
Huete A, Didan K, Miura T, Rodriquez E, Gao X, Ferreira L (2002) Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens Environ 83:195–213
Lewis PA, DeLoach CJ, Knutson AE, Tracy JL, Robbins TO (2003) Biology of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae), an Asian leaf beetle for biological control of saltcedars (Tamarix spp.) in the United States. Biol Control 27:101–116
Litt AR, Provencher L, Tanner GW, Franz R (2001) Herpetofaunal responses to restoration treatments of longleaf pine sandhills in Florida. Restor Ecol 9:462–474
Merritt DM, Shafroth PB (2012) Edaphic, salinity, and stand structural trends in chronosequences of native and non-native dominated riparian forests along the Colorado River, USA. Biol Invasions 14:2665–2685
Nagler PL, Brown T, Hultine KR, van Riper IIIC et al (2012) Regional scale impacts of Tamarix leaf beetles (Diorhabda carinulata) on the water availability of western U.S. rivers as determined by multi-scale remote sensing methods. Remote Sens Environ 118:227–240
Nagler PL, Pearlstein S, Glenn EP, Brown T, Bateman HL, Bean DW, Hultine KR (2014) Rapid dispersal of saltcedar (Tamarix spp.) biocontrol beetles (Diorhabda carinulata) on a desert river detected by phenocams, MODIS imagery and ground observations. Remote Sens Environ 140:206–219
Nielsen DP, Bateman HL (2013) Population metrics and habitat utilization of common side-blotched lizards (Uta stansburiana) in saltcedar (Tamarix) habitat. Southwest Nat 58:28–34
Oak Ridge National Laboratory (ORNL) Distributed Active Archive Center (2013) MODIS subsetted land products, collection 5. Oak Ridge, Tennessee: ORNL DAAC http://daac.ornl.gov/MODIS/modis.html
Paxton EH, Theimer TC, Sogge MK (2011) Biocontrol of exotic tamarisk: potential demographic consequences for riparian birds in the southwestern United States. Condor 113:255–265
Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298
Pike DA, Webb JK, Shine R (2011) Removing forest canopy cover restores a reptile assemblage. Ecol Apps 21:271–280
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria www.R-project.org
Rouag R, Berrahma I, Luiselli L (2006) Food habits and daily activity patterns of the North African ocellated lizard Timon pater from northeastern Algeria. J Nat Hist 40:1369–1379
Sabo JL, Power ME (2002) River-watershed exchanged: effects on riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1860–1869
Shafroth PB, Cleverly JR, Dudley TL, Taylor JP et al (2005) Control of Tamarix in the western United States: implications for water salvage, wildlife use, and riparian restoration. Environ Manag 35:231–246
Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808–1817
Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974
Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899
Smith WH, Rissler LJ (2010) Quantifying disturbance in terrestrial communities: abundance-biomass comparisons of herpetofauna closely track forest succession. Restor Ecol 18:195–204
Snyder KA, Scott RL, McGwire K (2012) Multiple year effects of a biological control agent (Diorhabda carinulata) on Tamarix (saltcedar) ecosystem exchanges of carbon dioxide and water. Agr Forest Meteorol 164:161–169
Sogge MK, Sferra SJ, Paxton EH (2008) Tamarix as habitat for birds: implications to riparian restoration in the southwestern United States. Restor Ecol 16:146–154
Sogge MK, Paxton EH, van Riper III C (2013) Tamarisk in riparian woodlands: a bird’s eye view. In: Sher A, Quigley M (eds) Tamarix: passenger vs. driver of ecological change. Oxford University Press, UK, pp 189–206
Steen DA, Smith LL, Morris G, Conner LM, Litt AR, Pokswinski S, Guyer C (2013) Response of six-lined racerunner (Aspidoscelis sexlineata) to habitat restoration in fire-suppressed longleaf pine (Pinus palustris) sandhills. Restor Ecol 21:457–463
Szaro RC, Belfit SC (1986) Herpetofaunal use of a desert riparian island and its adjacent scrub habitat. J Wildl Manag 50:752–761
Tan B, Woodcock CE, Hu J, Zhang P, Ozdogan M, Huang D, Yang W, Knyazikhin Y, Myneni RB (2006) The impact of gridding artifacts on the local spatial properties of MODIS data: implications for validation, compositing, and band-to-band registration across resolutions. Remote Sens Environ 105:98–114
Tracy JT, Robbins TO (2009) Taxonomic revision and biogeography of the Tamarix feeding Diorhabda elongata (Brullé, 1832) species group (Coleoptera: Chrysomelidae: Galerucinae: Galerucini) and analysis of their potential in biological control of Tamarisk. Zootaxa 2101:1–152
van Riper C, Paxton KL, O’Brien C, Shafroth PB, McGrath LJ (2008) Rethinking avian response to Tamarix on the lower Colorado River: a threshold hypothesis. Restor Ecol 16:155–167
Waichman AV (1992) An alphanumeric code for toe clipping amphibians and reptiles. Herpetol Rev 23:19–21
Acknowledgments
We thank the Bureau of Land Management in Nevada and Arizona for permitting access to study sites. We thank Aaron Switalski, Michael Bonacci, Rachel Olzer, Nick Vandehei, Rachael Cernetic, Danny Nielsen, Steven Anderson, Michael Cleaver, Paul Maier, Jean Galang, and William Bubnis for field assistance. We thank Tom Dudley and Michael Kuehn for logistical support. We thank Melanie Banville for help with R code. Permits were issued by the Arizona Game and Fish Department, Nevada Department of Wildlife, and Institutional Animal Care and Use Committee. Funding for H.L.B. has come from the Department of Applied Sciences and Mathematics at Arizona State University. Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. government.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bateman, H.L., Merritt, D.M., Glenn, E.P. et al. Indirect effects of biocontrol of an invasive riparian plant (Tamarix) alters habitat and reduces herpetofauna abundance. Biol Invasions 17, 87–97 (2015). https://doi.org/10.1007/s10530-014-0707-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-014-0707-0